Phylogenetic diversity of NO reductases, new tools for <i>nor</i> monitoring, and insights into N<sub>2</sub>O production in natural and engineered environments

doi:10.1007/s11783-022-1562-3

Front. Environ. Sci. Eng.

2022, Vol. 16

Issue (10) : 127 https://doi.org/10.1007/s11783-022-1562-3

RESEARCH ARTICLE

Phylogenetic diversity of NO reductases, new tools for nor monitoring, and insights into N₂O production in natural and engineered environments

Sung-Geun Woo^1,²(

), Holly L. Sewell¹, Craig S. Criddle^1,²

¹. Department of Civil and Environmental Engineering, Stanford University, Stanford, CA 94305, USA
². NSF Engineering Research Center, Re-Inventing the Nation’s Urban Water Infrastructure (ReNUWIt), Stanford University, Stanford, CA 94305, USA

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Abstract

● 548 representative nor genes were collected to create complete phylogenetic trees.

● The distribution of nor and nod genes were detected in 18 different phyla.

● The most conserved amino acids in NOR were located adjacent to the active site.

● nor-universal and Clade-specific primers were designed, suggested, and tested.

Nitric oxide reductases (NORs) have a central role in denitrification, detoxification of nitric oxide (NO) in host-pathogen interactions, and NO-mediated cell-cell signaling. In this study, we focus on the phylogeny and detection of qNOR and cNOR genes because of their nucleotide sequence similarity and evolutionary relatedness to cytochrome oxidases, their key role in denitrification, and their abundance in natural, agricultural, and wastewater ecosystems. We also include nitric oxide dismutase (NOD) due to its similarity to qNOR. Using 548 nor sequences from publicly accessible databases and sequenced isolates from N₂O-producing bioreactors, we constructed phylogenetic trees for 289 qnor/nod genes and 259 cnorB genes. These trees contain evidence of horizontal gene transfer and gene duplication, with 13.4% of the sequenced strains containing two or more nor genes. By aligning amino acid sequences for qnor + cnor, qnor, and cnor, we identified four highly conserved regions for NOR and NOD, including two highly conserved histidine residues at the active site for qNOR and cNOR. Extending this approach, we identified conserved sequences for: 1) all nor (nor-universal); 2) all qnor (qnor-universal) and all cnor (cnor-universal); 3) qnor of Comamonadaceae; 4) Clade-specific sequences; and 5) nod of Candidatus Methylomirabilis oxyfera. Examples of primer performance were confirmed experimentally.

Keywords N₂O Greenhouse gas NO reductase NO dismutase Primer Crystal structure

Corresponding Author(s): Sung-Geun Woo

Issue Date: 17 March 2022

Cite this article:

Sung-Geun Woo,Holly L. Sewell,Craig S. Criddle. Phylogenetic diversity of NO reductases, new tools for nor monitoring, and insights into N₂O production in natural and engineered environments[J]. Front. Environ. Sci. Eng., 2022, 16(10): 127.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-022-1562-3
https://academic.hep.com.cn/fese/EN/Y2022/V16/I10/127

Fig.1 Crystal structures of qNOR (left) from Neisseria meningitidis alpha14 (6L1X) and cNOR (right) from Pseudomonas aeruginosa PAO1 (5GUW). The top two panels show profile views of NOR with a top segment located within the periplasmic space and alpha helices spanning the cytoplasmic membrane and extending into the cytoplasm. Primers in this study for qnor and cnor universal (qcU), qnor-universal (qU), and cnor-universal (cU) based on the conserved amino acids are shown in red, green and blue, respectively. The bottom two panels show views looking up into the transmembrane helices from inside the cytoplasm. Roman numerals indicate transmembrane domains.

Fig.2 qnor + cnorC and qnor + cnorB nucleotide sequence alignments. The colored nucleotide positions represent 95% conserved nucleotides across all 548 qnor + cnor sequences (Red: A, Yellow: G, Green: T, Blue: C). α-helices and β-sheets are indicated with blue boxes and orange arrows, respectively. The α4 helix between alignments for cnorC + qnor and cnorB + qnor was omitted, and TM XIV (i.e., TM XII of cNOR) at the end of the sequence are not shown.

Fig.3 qnor and cnor nucleotide sequence alignments. The colored nucleotide positions represent 99% conserved nucleotides across all 289 qnor or 259 cnor sequences (Red: A, Yellow: G, Green: T, Blue: C).

Tab.1 Conserved amino acids and primer sets for qnor + cnor (nor-universal, qcU) designed in this study

Fig.4 Evolutionary relationship of 289 qnor and 259 cnorB using the maximum likelihood method. Four qnor sequences and one cnor sequence (marked with red dots) are from the sequenced genomes of N₂O-producing bioreactor isolates. All other sequences were obtained from databases.

Tab.2 Application of newly designed nor-universal (qcU), qnor and cnor Clade-specific (based on qnor-universal (qU) and cnor-universal (cU) primers), and Comamonadaceae-specific (qSComa1R) primer sets to pure strains

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